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Dispersal is a fundamental process in the functioning of animal societies as it regulates the degree to which closely related individuals are spatially concentrated. A species' dispersal pattern can be complex as it emerges from individuals' decisions shaped by the cost-benefit tradeoffs associated with either remaining in the natal group or dispersing. Given the potential complexity, combining long-term demographic information with molecular data can provide important insights into dispersal patterns of a species. Based on a 15-year study that integrates multiyear demographic data on six groups with longitudinal and cross-sectional genetic sampling of 20 groups (N = 169 individuals, N = 21 polymorphic microsatellite loci), we describe the various dispersal strategies of male and female black howler monkeys (Alouatta pigra) inhabiting Palenque National Park, Mexico. Genetically confirmed dispersal events (N = 21 of 59 males; N = 6 of 65 females) together with spatial autocorrelation analyses revealed that the dispersal pattern of black howlers is bisexual with strong sex-biases in both dispersal rate (males disperse more often than females) and dispersal distance (females disperse farther than males). Observational and genetic data confirm that both males and females can successfully immigrate into established groups, as well as form new groups with other dispersing individuals. Additionally, both males and females may disperse singly, as well as in pairs, and both may also disperse secondarily. Overall, our findings suggest multiple dispersal trajectories for black howler males and females, and longer multiyear studies are needed to unravel which demographic, ecological and social factors underlie individuals' decisions about whether to disperse and which dispersal options to take.
La dispersión es un proceso fundamental en el funcionamiento de las sociedades animales, ya que regula el grado en que los individuos parentados se concentran espacialmente. El patrón de dispersión de una especie puede ser complejo ya que surge de las decisiones de los individuos conformadas por las compensaciones de costo-beneficio asociadas con permanecer en el grupo natal o dispersarse. Dada esta posible complejidad, la combinación de información demográfica a largo plazo con datos moleculares puede proporcionar información importante sobre los patrones de dispersión de una especie en particular. Basado en un estudio de 15 años que integra datos demográficos de seis grupos sociales con muestreo genético longitudinal y transversal de 20 grupos (N = 169 individuos, N = 21 loci de microsatélites polimórficos), describimos las diversas estrategias de dispersión de machos y hembras del mono aullador negro (Alouatta pigra) que habitan el Parque Nacional Palenque, México. Los eventos de dispersión confirmados genéticamente (N = 21 de 59 machos; N = 6 de 65 hembras), junto con los análisis de autocorrelación espacial revelaron que el patrón de dispersión de los monos aulladores negros es bisexual con fuertes sesgos sexuales en ambas tasas de dispersión (los machos se dispersan más a menudo que las hembras) y distancia de dispersión (las hembras se dispersan más lejos que los machos). Los datos de observación y genéticos confirman que tanto machos como hembras pueden inmigrar con éxito a grupos ya establecidos, así como formar nuevos grupos con otros individuos que se están dispersando. Además, tanto los machos como las hembras pueden dispersarse individualmente, así como en parejas, y ambos también pueden dispersarse secundariamente. En general, nuestros hallazgos sugieren múltiples trayectorias de dispersión para aulladores negros de los dos sexos, y se necesitan más estudios para desentrañar qué factores demográficos, ecológicos y sociales subyacen en las decisiones de los individuos sobre si dispersarse y qué opciones de dispersión tomar.
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Alouatta , Alouatta/genética , Animales , Estudios Transversales , Demografía , Femenino , Masculino , MéxicoRESUMEN
A recent focus in community ecology has been on how within-species variability shapes interspecific niche partitioning. Primate color vision offers a rich system in which to explore this issue. Most neotropical primates exhibit intraspecific variation in color vision due to allelic variation at the middle-to-long-wavelength opsin gene on the X chromosome. Studies of opsin polymorphisms have typically sampled primates from different sites, limiting the ability to relate this genetic diversity to niche partitioning. We surveyed genetic variation in color vision of five primate species, belonging to all three families of the primate infraorder Platyrrhini, found in the Yasuní Biosphere Reserve in Ecuador. The frugivorous spider monkeys and woolly monkeys (Ateles belzebuth and Lagothrix lagotricha poeppigii, family Atelidae) each had two opsin alleles, and more than 75% of individuals carried the longest-wavelength (553-556 nm) allele. Among the other species, Saimiri sciureus macrodon (family Cebidae) and Pithecia aequatorialis (family Pitheciidae) had three alleles, while Plecturocebus discolor (family Pitheciidae) had four alleles-the largest number yet identified in a wild population of titi monkeys. For all three non-atelid species, the middle-wavelength (545 nm) allele was the most common. Overall, we identified genetic evidence of fourteen different visual phenotypes-seven types of dichromats and seven trichromats-among the five sympatric taxa. The differences we found suggest that interspecific competition among primates may influence intraspecific frequencies of opsin alleles. The diversity we describe invites detailed study of foraging behavior of different vision phenotypes to learn how they may contribute to niche partitioning.
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In group-living species, integrating into a new social group after dispersal is an important life history milestone associated with physical and social challenges. Generally, this process seems to be accompanied by heightened glucocorticoid (GC) concentrations; however, most studies of physiological responses to group transfer have been conducted on species with despotic social relationships, where integrating individuals are often targets of frequent aggression. Here we present data on fecal glucocorticoid (fGC) concentrations during periods of unstable group membership for male woolly monkeys (Lagothrix lagotricha poeppigii), a species with extremely low rates of male-male aggression and generally tolerant male-male associations. We collected data on males in four study groups at the Tiputini Biodiversity Station, Ecuador, and observed three attempted transfer events, involving a total of four adult males, in one study group. We observed only three instances of overt aggression (chases) between males across the entire study period, though male display behaviors were more frequent. We tested whether rates of displays were higher during periods of unstable group membership using a generalized linear mixed model (LMM). We also examined whether male status, group stability, and the occurrence of intergroup encounters affected fGC concentrations using LMMs. Contrary to our predictions, rates of display behaviors were not higher during periods of unstable group membership. However, both transient/integrating males and those who were already group members showed elevated fGC concentrations during these unstable periods. Our results suggest that even in species with tolerant male-male relationships, the integration of unfamiliar individuals can provoke an increase in GCs.
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Atelinae , Agresión , Animales , Ecuador , Procesos de Grupo , MasculinoRESUMEN
Patterns of ranging behavior and space use are key for evaluating current ideas about the evolution and maintenance of pair-living and sexual monogamy as they provide insights into the dispersion of females, the potential for territoriality, and whether males are limited to defending an area that can support only one female and her offspring. We examined ranging behavior and space use to evaluate the potential for territoriality in five groups of red titi monkeys (Plecturocebus discolor) during a 10-year study in Ecuadorian Amazonia. Mean home range size, calculated using a time-sensitive local convex hull estimation procedure, was 4.0 ± 1.4 ha. Annual home ranges of neighboring groups overlapped, on average, 0%-7%. Mean daily path length was 670 ± 194 m, resulting in defendability indices of 2.2-3.6 across groups. Groups visited, on average, 4 of 12 sections of their home range border area per day, but that was not more often than would be expected by chance, and intergroup encounters were infrequent. We did not find evidence of active monitoring for intruders in border areas, in that groups did not travel either faster or slower when at the border than when in central areas of their range. The absence of overt monitoring might be compensated for by engaging in loud calls, which the study groups did throughout their home ranges; these calls may serve as an advertisement of occupancy and a deterrent to intruding conspecifics. Our finding that red titis have a high potential for territoriality is consistent with several of the main hypotheses proposed to explain pair-living in mammals.
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Pitheciidae , Territorialidad , Animales , Brasil , Callicebus , Femenino , Fenómenos de Retorno al Lugar Habitual , MasculinoRESUMEN
With their large body size and "slow" life histories, atelin primates are thought to follow a risk-averse breeding strategy, similar to capital breeders, in which they accumulate energy reserves in anticipation of future reproductive events such as gestation and lactation. However, given the paucity of longitudinal data from wild populations, few studies to date have been able to compare the timing of reproductive events (e.g., copulations, conceptions, and births) in relation to shifting resource availability over multiple years. We examined the reproductive patterns of two atelin species-white-bellied spider monkeys (Ateles belzebuth) and lowland woolly monkeys (Lagothrix lagotricha poeppigii)-in relation to habitat-wide estimates of fruit availability at the Tiputini Biodiversity Station (TBS) in Amazonian Ecuador. Our sample included 4 years of data on births (N = 36) and copulations (N = 170) for Lagothrix, 10 years of data on births (N = 35) and copulations (N = 74) for Ateles, and 7 years of data on ripe fruit availability. Reproductive events were distinctly seasonal. For both species, births were concentrated between May and September, a time period in which ripe fruit was relatively scarce, while inferred conceptions occurred between September and January, when ripe fruit availability was increasing and maintained at high-levels throughout the forest. Interannual variation in births was relatively stable, except for in 2016 when twice as many infants were born following a strong El Niño event that may have led to unusually high levels of fruit productivity during the 2015 breeding season. Although copulations were observed year-round, an overwhelming majority (>90% for Lagothrix and >80% for Ateles) took place between August and February when females were most likely to conceive. Collectively, these data follow the reproductive patterns observed in other atelin primates, and, as proposed by others, suggest that atelins may follow a risk-averse breeding strategy.
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Atelinae/fisiología , Reproducción , Conducta Sexual Animal , Animales , Ecuador , Femenino , Frutas , Masculino , Estaciones del Año , SimpatríaRESUMEN
The carbon sink capacity of tropical forests is substantially affected by tree mortality. However, the main drivers of tropical tree death remain largely unknown. Here we present a pan-Amazonian assessment of how and why trees die, analysing over 120,000 trees representing > 3800 species from 189 long-term RAINFOR forest plots. While tree mortality rates vary greatly Amazon-wide, on average trees are as likely to die standing as they are broken or uprooted-modes of death with different ecological consequences. Species-level growth rate is the single most important predictor of tree death in Amazonia, with faster-growing species being at higher risk. Within species, however, the slowest-growing trees are at greatest risk while the effect of tree size varies across the basin. In the driest Amazonian region species-level bioclimatic distributional patterns also predict the risk of death, suggesting that these forests are experiencing climatic conditions beyond their adaptative limits. These results provide not only a holistic pan-Amazonian picture of tree death but large-scale evidence for the overarching importance of the growth-survival trade-off in driving tropical tree mortality.
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Ecología , Bosques , Árboles/crecimiento & desarrollo , Biomasa , Brasil , Dióxido de Carbono , Secuestro de Carbono , Ecosistema , Monitoreo del Ambiente , Modelos Biológicos , Modelos de Riesgos Proporcionales , Factores de Riesgo , Clima TropicalRESUMEN
The taxonomy of muriquis,â¯the largest extant primates in the New World,â¯is controversial. While some specialists argue for a monotypic genus (Brachyteles arachnoides), others favor a two-species classification, splitting northern muriquis (Brachyteles hypoxanthus) from southern muriquis (B. arachnoides). This uncertainty affects how we study the differences between these highly endangered and charismatic primates, as well as the design of more effective conservation programs. To address this issue, between 2003 and 2017 we collected over 230 muriqui fecal samples across the genus' distribution in the Brazilian Atlantic Forest, extracted DNA from these samples, and sequenced 423 base pairs of the mitochondrial DNA (mtDNA) control region. Phylogenetic and species delimitation analyses of our sequence dataset robustly support two reciprocally monophyletic groups corresponding to northern and southern muriquis separated by an average 12.7% genetic distance. The phylogeographic break between these lineages seems to be associated with the Paraíba do Sul River and coincides with the transition between the north and south Atlantic Forest biogeographic zones. Published divergence estimates from whole mitochondrial genomes and nuclear loci date the split between northern and southern muriquis to the Early Pleistocene (ca. 2.0 mya), and our new mtDNA dataset places the coalescence time for each of these two clades near the last interglacial (ca. 120-80 kya). Our results, together with both phenotypic and ecological differences, support recognizing northern and southern muriquis as sister species that should be managed as distinct evolutionarily significant units. Given that only a few thousand muriquis remain in nature, it is imperative that conservation strategies are tailored to protect both species from extinction.
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Atelinae/genética , Variación Genética , Atelinae/clasificación , Brasil , ADN Mitocondrial/análisis , Especies en Peligro de Extinción , Heces/química , FilogeografíaRESUMEN
We examined photic and ecological factors related to initiation of feeding by four sympatric primates in the rain forest of Amazonian Ecuador. With rare exceptions, morning activities of all taxa began only after the onset of nautical twilight, which occurred 47-48 min before sunrise. The larger spider and woolly monkeys, Ateles belzebuth and Lagothrix lagotricha poeppigii, left their sleeping trees before sunrise about half the time, while the smaller sakis and titi monkeys, Pithecia aequatorialis and Plecturocebus (formerly Callicebus) discolor, did not emerge until sunrise or later. None of the four taxa routinely began feeding before sunrise. Pithecia began feeding a median 2.17 h after sunrise, at least 0.8 h later than the median feeding times of the other three taxa. The early movement of Ateles and Lagothrix, and late initiation of feeding by Pithecia are consistent with temporal niche partitioning. Among most New World primate species, all males and many females, have dichromatic color vision, with only two cone photopigments, while some females are trichromats with three cone photopigments. Current evidence indicates that the dichromats have a foraging advantage in dim light, which could facilitate utilization of twilight periods and contribute to temporal niche partitioning. However, in our study, dichromatic males did not differentially exploit the dim light of twilight, and times of first feeding bouts of female Ateles and Lagothrix were similar to those of males. First feeding bouts followed a seasonal pattern, occurring latest in May-August, when ripe fruit abundance and ambient temperature were both relatively low. The most frugivorous taxon, Ateles, exhibited the greatest seasonality, initiating feeding 1.4 h later in May-August than in January-April. This pattern may imply a strategy of conserving energy when ripe fruit is scarcer, but starting earlier to compete successfully when fruit is more abundant. Lower temperatures were associated with later feeding of Ateles (by 26 min / °C) and perhaps Pithecia, but not Lagothrix or Plecturocebus. The potential for modification of temporal activity patterns and temporal niche partitioning by relatively small changes in temperature should be considered when predicting the effects of climate change.
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Atelinae/fisiología , Ecología , Conducta Alimentaria/fisiología , Pitheciidae/fisiología , Árboles/fisiología , Clima Tropical , Animales , Atelinae/clasificación , Ecuador , Femenino , Frutas/crecimiento & desarrollo , Masculino , Estimulación Luminosa , Pitheciidae/clasificación , Estaciones del Año , Luz Solar , Simpatría , Factores de TiempoRESUMEN
OBJECTIVES: Territoriality refers to the consistent defense of an area within the home range (HR) against intrusions of conspecifics. It implies exclusive space use with low degree of overlap among neighboring groups, high site fidelity, specific ranging behavior such as high mobility relative to HR size and frequent visits of territory borders, and monitoring behavior. We examined ranging behavior and use of space to evaluate territoriality in Pithecia aequatorialis in Ecuador. MATERIALS AND METHODS: Between 2005 and 2015, we monitored one main study group continuously and five additional groups for shorter periods (5 months to 2.5 years) at the Tiputini Biodiversity Station, in eastern Ecuador. We scored the location of the study groups at 20 min intervals during, on average, 5 days per month. We estimated saki HRs and core areas (CAs) using the fixed kernel density method (95 and 50%, respectively). RESULTS: The average HR size was 57 ha and the average CA 14 ha. The degree of overlap between HRs of neighboring groups was low (2-9%). For the main study group, the average overlap between annual HRs was 82%. Mean daily path length across groups was 1,151 m; the defensibility index varied between 1.1 and 2.3 (values >1 are suggestive of territoriality), and the fractional monitoring rate varied between 0.06 and 0.15 (values >0.08 are suggestive of territoriality). Groups did not visit their HR borders (100 m inner buffer) more often than would be expected by chance. Travel speed and directness were comparable between the borders and the centers of groups' HRs. DISCUSSION: Our multiyear study suggests that equatorial sakis show low degree of range overlap and high site fidelity and have the potential to be territorial, given their high mobility relative to HR size that allows for frequent border monitoring. Nevertheless, their movement patterns in border areas did not reveal evidence for monitoring behavior.
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Fenómenos de Retorno al Lugar Habitual/fisiología , Pitheciidae/fisiología , Territorialidad , Animales , Antropología Física , Ecuador , Femenino , MasculinoRESUMEN
Long-range vocal communication in socially monogamous titi monkeys is mediated by the production of loud, advertising calls in the form of solos, duets, and choruses. We conducted a power spectral analysis of duets and choruses (simply "duets" hereafter) followed by linear discriminant analysis using three acoustic parameters-dominant frequency of the combined signal, duet sequence duration, and pant call rate-comparing the coordinated vocalizations recorded from 36 family groups at 18 sites in Bolivia, Peru and Ecuador. Our analysis identified four distinct duetting patterns: (1) a donacophilus pattern, sensu largo, characteristic of P. donacophilus, P. pallescens, P. olallae, and P. modestus; (2) a moloch pattern comprising P. discolor, P. toppini, P. aureipalatii, and P. urubambensis; (3) a torquatus pattern exemplified by the duet of Cheracebus lucifer; and (4) the distinctive duet of P. oenanthe, a putative member of the donacophilus group, which is characterized by a mix of broadband and narrowband syllables, many of which are unique to this species. We also document a sex-related difference in the bellow-pant phrase combination among the three taxa sampled from the moloch lineage. Our data reveal a presumptive taxonomic incoherence illustrated by the distinctive loud calls of both P. urubambensis and P. oenanthe within the donacophilus lineage, sensu largo. The results are discussed in light of recent reassessments of the callicebine phylogeny, based on a suite of genetic studies, and the potential contribution of environmental influences, including habitat acoustics and social learning. A better knowledge of callicebine loud calls may also impact the conservation of critically endangered populations, such as the vocally distinctive Peruvian endemic, the San Martin titi, P. oenanthe.
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Species-specific demographic parameters and life history variables are important for understanding how individual primate taxa have adapted to evolutionary and ecological pressures and for conducting interspecific comparisons as well as for conducting population viability analyses and for managing captive populations. Here, we describe results from a 12+ year study of the demographic dynamics of a wild group of white-bellied spider monkeys (Ateles belzebuth belzebuth) living near the Tiputini Biodiversity Station in a largely pristine rainforest in western Amazonia. Across the study period, group size varied between 25 and 37 individuals, and there was a clearly female-biased sex ratio within all age classes. Females were the dispersing sex, as 19 females born into the group disappeared close to reaching adult body size and were presumed to have emigrated, while seven subadult or adult females joined the group during the study period. We estimated the age of dispersal for females at 5.9 ± SD 0.4 years (N = 13). Our study confirms that males are the philopatric sex, as all natal males have remained in the group and some have begun to reproduce, while no males have immigrated. Males began ranging independently from their mothers at â¼4.5 years of age and began copulating with adult females by the age of â¼5 years. Females had long inter-birth intervals (44.2 ± SD 7.8 months; range: 32-64 months, N = 21). Based on our data, female spider monkeys might have longer life spans than males, as only one out of six adult males but 9 out of 11 adult females present in the group in mid 2005 were still present in January 2018. The slow development and extended life histories of wild spider monkeys pose significant challenges for the ability of these primates to cope with habitat degradation and hunting throughout their geographical distribution.
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Groups of animals (including humans) may show flexible grouping patterns, in which temporary aggregations or subgroups come together and split, changing composition over short temporal scales, (i.e. fission and fusion). A high degree of fission-fusion dynamics may constrain the regulation of social relationships, introducing uncertainty in interactions between group members. Here we use Shannon's entropy to quantify the predictability of subgroup composition for three species known to differ in the way their subgroups come together and split over time: spider monkeys (Ateles geoffroyi), chimpanzees (Pan troglodytes) and geladas (Theropithecus gelada). We formulate a random expectation of entropy that considers subgroup size variation and sample size, against which the observed entropy in subgroup composition can be compared. Using the theory of set partitioning, we also develop a method to estimate the number of subgroups that the group is likely to be divided into, based on the composition and size of single focal subgroups. Our results indicate that Shannon's entropy and the estimated number of subgroups present at a given time provide quantitative metrics of uncertainty in the social environment (within which social relationships must be regulated) for groups with different degrees of fission-fusion dynamics. These metrics also represent an indirect quantification of the cognitive challenges posed by socially dynamic environments. Overall, our novel methodological approach provides new insight for understanding the evolution of social complexity and the mechanisms to cope with the uncertainty that results from fission-fusion dynamics.
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Atelinae/fisiología , Pan troglodytes/fisiología , Conducta Social , Theropithecus/fisiología , Animales , Conducta Animal , IncertidumbreRESUMEN
Phylogenetic relationships amongst the robust capuchin monkeys (genus Sapajus) are poorly understood. Morphology-based taxonomies have recognized anywhere from one to twelve different species. The current IUCN (2017) classification lists eight robust capuchins: S. xanthosternos, S. nigritus, S. robustus, S. flavius, S. libidinosus, S. cay, S. apella and S. macrocephalus. Here, we assembled the first phylogenomic data set for Sapajus using ultra-conserved elements (UCEs) to reconstruct a capuchin phylogeny. All phylogenomic analyses strongly supported a deep divergence of Sapajus and Cebus clades within the capuchin monkeys, and provided support for Sapajus nigritus, S. robustus and S. xanthosternos as distinct species. However, the UCE phylogeny lumped the putative species S. cay, S. libidinosus, S. apella, S. macrocephalus, and S. flavius together as a single widespread lineage. A SNP phylogeny constructed from the UCE data was better resolved and recovered S. flavius and S. libidinosus as sister species; however, S. apella, S. macrocephalus, and S. cay individuals were recovered in two geographic clades, from northeastern and southwestern Amazon, rather than clustering by currently defined morphospecies. STRUCTURE analysis of population clustering revealed widespread admixture among Sapajus populations within the Amazon and even into the Cerrado and Atlantic Forest. Difficulty in assigning species by morphology may be a result of widespread population admixture facilitated through frequent movement across major rivers and even ecosystems by robust capuchin monkeys.
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Cebus/clasificación , Cebus/genética , Pool de Genes , Genómica , Filogenia , Animales , Calibración , Cebinae , Ecosistema , Genética de Población , Geografía , Funciones de Verosimilitud , Polimorfismo de Nucleótido Simple/genética , América del SurRESUMEN
Nonhuman primates, our closest biological relatives, play important roles in the livelihoods, cultures, and religions of many societies and offer unique insights into human evolution, biology, behavior, and the threat of emerging diseases. They are an essential component of tropical biodiversity, contributing to forest regeneration and ecosystem health. Current information shows the existence of 504 species in 79 genera distributed in the Neotropics, mainland Africa, Madagascar, and Asia. Alarmingly, ~60% of primate species are now threatened with extinction and ~75% have declining populations. This situation is the result of escalating anthropogenic pressures on primates and their habitats-mainly global and local market demands, leading to extensive habitat loss through the expansion of industrial agriculture, large-scale cattle ranching, logging, oil and gas drilling, mining, dam building, and the construction of new road networks in primate range regions. Other important drivers are increased bushmeat hunting and the illegal trade of primates as pets and primate body parts, along with emerging threats, such as climate change and anthroponotic diseases. Often, these pressures act in synergy, exacerbating primate population declines. Given that primate range regions overlap extensively with a large, and rapidly growing, human population characterized by high levels of poverty, global attention is needed immediately to reverse the looming risk of primate extinctions and to attend to local human needs in sustainable ways. Raising global scientific and public awareness of the plight of the world's primates and the costs of their loss to ecosystem health and human society is imperative.
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Cercopithecidae , Ecosistema , Extinción Biológica , AnimalesRESUMEN
Lineages tend to retain ecological characteristics of their ancestors through time. However, for some traits, selection during evolutionary history may have also played a role in determining trait values. To address the relative importance of these processes requires large-scale quantification of traits and evolutionary relationships among species. The Amazonian tree flora comprises a high diversity of angiosperm lineages and species with widely differing life-history characteristics, providing an excellent system to investigate the combined influences of evolutionary heritage and selection in determining trait variation. We used trait data related to the major axes of life-history variation among tropical trees (e.g. growth and mortality rates) from 577 inventory plots in closed-canopy forest, mapped onto a phylogenetic hypothesis spanning more than 300 genera including all major angiosperm clades to test for evolutionary constraints on traits. We found significant phylogenetic signal (PS) for all traits, consistent with evolutionarily related genera having more similar characteristics than expected by chance. Although there is also evidence for repeated evolution of pioneer and shade tolerant life-history strategies within independent lineages, the existence of significant PS allows clearer predictions of the links between evolutionary diversity, ecosystem function and the response of tropical forests to global change.
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Bosques , Filogenia , Árboles/clasificación , Clima Tropical , Evolución Biológica , Ecología , América del SurRESUMEN
Understanding the processes that determine above-ground biomass (AGB) in Amazonian forests is important for predicting the sensitivity of these ecosystems to environmental change and for designing and evaluating dynamic global vegetation models (DGVMs). AGB is determined by inputs from woody productivity [woody net primary productivity (NPP)] and the rate at which carbon is lost through tree mortality. Here, we test whether two direct metrics of tree mortality (the absolute rate of woody biomass loss and the rate of stem mortality) and/or woody NPP, control variation in AGB among 167 plots in intact forest across Amazonia. We then compare these relationships and the observed variation in AGB and woody NPP with the predictions of four DGVMs. The observations show that stem mortality rates, rather than absolute rates of woody biomass loss, are the most important predictor of AGB, which is consistent with the importance of stand size structure for determining spatial variation in AGB. The relationship between stem mortality rates and AGB varies among different regions of Amazonia, indicating that variation in wood density and height/diameter relationships also influences AGB. In contrast to previous findings, we find that woody NPP is not correlated with stem mortality rates and is weakly positively correlated with AGB. Across the four models, basin-wide average AGB is similar to the mean of the observations. However, the models consistently overestimate woody NPP and poorly represent the spatial patterns of both AGB and woody NPP estimated using plot data. In marked contrast to the observations, DGVMs typically show strong positive relationships between woody NPP and AGB. Resolving these differences will require incorporating forest size structure, mechanistic models of stem mortality and variation in functional composition in DGVMs.
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Biomasa , Bosques , Modelos Teóricos , Árboles/crecimiento & desarrollo , Clima Tropical , América del SurRESUMEN
We investigated demographic patterns and life history traits from several groups of red titi monkeys (Callicebus discolor) and equatorial sakis (Pithecia aequatorialis) monitored throughout the first 12 years (November 2003 through May 2015) of an ongoing research project in the Yasuní National Park and Biosphere Reserve, Ecuador. The saki groups ranged in size between two and six individuals, comprising either one adult male and one adult female or multiple adult-sized males or females, plus immatures. Deviations from a pair-living structure resulted when two different daughters of the resident female grew up and successfully reproduced in their natal group and when an adult-sized male temporarily immigrated into the group when it already contained an adult male. The titi groups also ranged in size between two and six individuals, but almost exclusively lived in groups with one adult individual of each sex. No titi offspring were observed to breed in their natal groups, and both male and female offspring dispersed when they were between 2.1 and 5.0 years old. In both titi and saki groups, vacant breeding positions resulting from the disappearance of an adult group member were promptly occupied by immigrants of the same sex as the disappeared group member. We recorded nine saki and 28 titi births. Eighty-three percent of the titi births occurred between September and January, suggesting reproductive seasonality. The mean interbirth interval after an infant survived its first 6 months was 21.3 ± SE 1.9 months (N = 3) for sakis and 14.5 ± SE 1.5 months (N = 14) for titis. Saki infant survival was 70%, and juvenile survival 57%. Titi infant survival was 88%, and juvenile survival was 53%. This 12-year study provides important insights into the functioning and maintenance of pair-living and social monogamy in two little-known platyrrhine species.
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Fenómenos de Retorno al Lugar Habitual , Pitheciidae/fisiología , Reproducción , Animales , Demografía , Ecuador , Femenino , Longevidad , Masculino , Estaciones del Año , Conducta Sexual Animal , Conducta Social , Especificidad de la EspecieRESUMEN
Titi monkeys (Callicebus spp.) are one of two primate genera that live almost exclusively in groups with one adult-size individual of each sex and exhibit extensive biparental care of offspring. We provide a quantitative description of infant care and pairmate behavior in natural groups of Callicebus discolor that contributes to a limited literature on the behavioral ecology of wild titi monkeys. We collected data during a 3-year period from two social groups living in primary tropical rainforest at the Tiputini Biodiversity Station in Amazonian Ecuador before and after the birth of five infants. In order to evaluate the potential social and energetic costs associated with biparental care of offspring, we examined the relationships between infant care, pairmate behavior, and adult activity budgets. We found that males were almost exclusively responsible for transporting, grooming, sharing food, and playing with infants. As predicted, we found that, following the birth of an infant, adults groomed their partners less, spent less time in contact, and that huddling between pairmates decreased. Contrary to our predictions, after the birth of an infant, females did not increase the time spent feeding, and males did not decrease the time spent moving nor increase their resting time. Overall, our data suggest that the pair may experience social costs during times of intense infant care but that any putative energetic costs associated with infant care are not mitigated by adjusting physical activity. Future studies should investigate energy intake and expenditure, and consider how the variation observed in pairmate social relationships may affect reproductive success.
Asunto(s)
Conducta Materna , Apareamiento , Conducta Paterna , Pitheciidae/fisiología , Conducta Social , Animales , Ecuador , Femenino , MasculinoRESUMEN
Saki monkeys live in socially monogamous groups and in groups containing more than one same-sex adult. As part of a 10-year study of equatorial sakis (Pithecia aequatorialis) in Ecuador, we documented the immigration of a second adult male into a group containing a resident male-female pair that had associated with one another for seven years and the resident female's two daughters. In the first month after immigration, the resident male spent more time closer to and grooming his putative adult daughter than the resident female, and the two males were seen performing a cooperative territorial display. After two months, the resident male interacted more with the resident female than with his putative adult daughter, while that daughter interacted more with the immigrant male and copulated with him. After three months, the males left the group together and associated with an unfamiliar female, leaving the resident females and a neonate behind. The resident male then paired with a new female, while the immigrant male joined another group, again as a second male. Compared to other socially monogamous primates, sakis appear to have a more variable social system whereby additional males can join established groups and form relationships with putatively unrelated males.
Asunto(s)
Pitheciidae/fisiología , Conducta Sexual Animal , Conducta Social , Animales , Ecuador , Femenino , Aseo Animal , Masculino , Pitheciidae/psicología , TerritorialidadRESUMEN
The taxonomic history of the genus Lagothrix is complex, with molecular and morphological assessments giving conflicting results for the separation between its taxa. Phylogeographic studies of the most widely distributed species, Lagothrix lagotricha, have only been attempted recently and are limited to few individuals per collection site, many of which were captive making their geographical origin dubious. There is debate regarding the possibility of raising subspecies of Lagothrix lagotricha to the species level, therefore the geographical origin of samples is particularly relevant. In the present work we revisit the intraspecific phylogeography of L. lagotricha from northwestern South America, including the subspecies L. l. poeppiggi, L. l. lagotricha and L. l. lugens (sensu Fooden, 1963), using DNA sequence data from hypervariable region I of the mitochondrial control region (D-loop HVI). Our results suggest a complex picture in which there are well delimited evolutionary units that, nonetheless, do not correlate well with the morphological variation used to support the current delimitation of taxa. Additionally, we corroborate previous results showing a lack of reciprocal monophyly between the putative subspecies of Lagothrix lagotricha, and we propose that this may be due to ancestral polymorphism that has been maintained following the recent spread of woolly monkeys throughout the western Amazonian lowlands and into the inter-Andean region of Colombia.